Reproducibility and normal values of static pupil diameters

Abstract

Purpose:

To provide additional information on normal values of static pupil diameter measurements for binocular infrared pupillometry with PupilX, a commercial pupillometer, and assess the reproducibility of this device’s measurements.

Methods:

The pupil diameters from 91 study participants with normal eyes with an average age of 39.7 years (SD 16.4 years) were measured with PupilX under scotopic (0 lx), mesopic (1 lx), and photopic (16 lx) illumination. To assess the repeatability of the device, each measurement was repeated 5 times.

Results:

The mean pupil diameters were 6.5 mm (SD 1.3 mm), 5.5 mm (SD 1.2 mm), and 4.03 mm (SD 0.9 mm) under scotopic, mesopic, and photopic illumination. Left and right eyes showed no difference in mean pupil diameters. The mean unsigned anisocoria was 0.26 mm (SD 0.32 mm) under scotopic, 0.26 mm (SD 0.27 mm) under mesopic, and 0.19 mm (SD 0.19 mm) under photopic illumination. The decrease in pupil diameter with age was largest for scotopic (≈0.057 mm/y) and smallest for photopic illumination (≈0.025 mm/y). The repeatability of the pupillometer was better than 0.2 mm.

Conclusions:

This study provides reference values for age- and light-related pupil diameters measured with the PupilX digital pupillometer in normal subjects.

Keywords

Age Brightness Normal values Pupillometry Reproducibility

Introduction

Reliable measurement of pupil diameters is of interest across the disciplines. The pupil diameter is influenced by many factors. It is primarily affected by adaptation to the brightness of illumination (1). Other effects that influence pupil size are age (1, 2), accommodation (1, 3), and cognitive effects. Cognitive effects such as emotional arousal (1, 4), mental activity (1, 5), and attention (1, 6) are relatively small and largely transient. Precise pupil diameter measurements (resolution <1 mm) with <1 second time resolution enable the study of these psychophysiologic effects (7). Measurement of pupil diameter and anisocoria is a standard diagnostic tool used before any refractive surgery or the implantation of multifocal intraocular lenses (IOLs) (8). The pupil diameter has a large effect on the optical transfer function of the eye (9) and directly affects the depth of field (10) and optical aberrations (11). The maximum scotopic pupil size should not be larger than the ablation zone in refractive surgery or the optics of a lens implant, otherwise ghost images and blurred vision (glare and halos) could be expected at low illumination (12, 13). Assessment of pupil size and dynamics might allow further IOL customization, especially for multifocal or aspheric IOLs (14), and customized laser in situ keratomileusis for presbyopia (15).

Pupil diameter and pupil dynamics measurements (pupillometry) also have potential for the diagnosis of diseases, such as primary angle closure glaucoma (16). Pupillometry might be used as a noninvasive, simple tool for additive detection of autonomic dysfunction in diabetes mellitus (17). However, there is no established measurement protocol to date for pupil size measurement, nor is there a gold standard pupillometer. Measurements vary in the choice of illumination reflecting mesopic and photopic conditions, the measurement protocol, and the technology being used for pupillometry (pupillometer and software). Standardization of pupil diameter measurements together with extensive studies of the pupil parameters in normal subjects is required to increase its diagnostic potential and accuracy.

Pupillometers measure pupil diameter by analyzing images of the pupil under specific illumination brightness. The measured pupil diameter refers to the entrance pupil, which is the virtual image of the physical pupil as seen through the cornea. Most pupillometers directly illuminate the pupil. The PupilX (Albomed GmbH) uses precisely calibrated indirect visible light illumination with white or colored light coupled with infrared imaging (880 nm wavelength) resulting in systematically higher pupil diameters (8). Imaging in infrared allows for measurement of the pupil diameter with any arbitrary illumination brightness, even in total darkness, using integrated infrared cameras (8). It has been seen that this produces less erroneous measurements than other established devices (Procyon and Colvard) (8). The width of the pupil is regulated through indirect visible illumination that can be applied to both eyes at once (binocular) or each eye individually (monocular). The illumination is applied through a 36 × 24 mm field, which corresponds to a field of view of 48° × 33° for each eye. Two focus-free video cameras capture images of both eyes simultaneously with an operating frequency of 30 frames per second (18). The pupil is detected and measured in real time with a spatial resolution of 45 μm per pixel (520 × 390 pixels) (18). The measurement range for pupil diameters goes from 1.5 mm to 9.0 mm. A close-fitting eye mask excludes ambient light, allowing pupillometry with precisely known illumination brightness.

Methods

The ethics committee approved the study, which adhered to the tenets of the Declaration of Helsinki. All 91 subjects provided informed consent prior to participation. Only subjects with normal eyes who were not taking medication and without any history of neurologic disease or brain injury were included in the study.

The pupil diameters of each subject were measured under 3 distinct illumination settings. The subjects were instructed to look straight forward and keep their eyes open during data acquisition. All measurements were executed by a trained ophthalmologist. The measurements took place in a darkened and quiet room in order to avoid distractions and unnecessary stray light using the PupilX pupillometer. The pupillometer was calibrated according to the manufacturer’s calibration protocol using targets (black circles) of known diameters (2 mm, 4 mm, 6 mm, 8 mm). Each measurement consists of 90 image frames taken within 3 seconds at a rate of 30 frames per second. The pupillometer’s software detects the pupil and reports the mean and standard deviations (SDs) of the 90 extracted pupil diameters. The 3 illumination settings were 0 lx (scotopic), 1 lx (mesopic), and 16 lx (photopic).

Before the first measurement, each subject stayed in the darkened room for ≥5 minutes to achieve dark adaptation of the pupil. Usually, the pupil diameter reaches its maximum within the first 2 minutes of dark adaptation (19). The first measurements were taken under scotopic illumination, followed by measurements under mesopic and finally photopic illumination. Both eyes were illuminated and measured at the same time with white light (LED, color temperature 6,500 K) of identical brightness. In between measurements, subjects were allowed to blink. They were also asked to reposition their head. Subjects were measured 5 times before moving on to the next illumination setting. At each new illumination setting, the subject’s eyes were given sufficient time to stabilize prior to measurement. Less than 30 seconds of adaptation time were usually sufficient for the pupil diameters to stabilize. In some cases it was not possible to collect 5 valid measurements for each of the 3 illumination settings; in those cases, the subject had to return another day to complete the measurement series. All measurements were completed within 2 months; subjects who did not have 5 successful measurements on the same day were excluded from the analysis of repeatability and internal consistency. The results of the PupilX measurements consist of 1 measurement series for each subject (Fig. 1). Each series contains 1 set of 5 measurements for each eye and illumination setting. The measurements include the mean pupil diameters (d) and the corresponding SDs (std).

Fig. 1

Graphic illustration of the intrasubject statistical analysis. Each measurement series consists of 3 measurement sets. Each set contains 5 measurements of 90 individual frames measured within 3 seconds for each eye with identical illumination. Anisocoria values are calculated for each set. The mean diameters d, their standard deviation (SD1), and the mean values of standard deviation (SD) are calculated for both eyes in each set individually. The relative pupil contractions are calculated based on the relative difference between the mean pupil diameters d for identical eyes.

The analysis of static pupil diameters in normal subjects proceeded in 2 steps (Fig. 1). First, the intrasubject statistics were calculated for each set. The intrasubject statistics include the mean value D of the pupil diameters (d), the corresponding SD (SD1), the mean STD of the standard deviations std. of the SDs, and the mean anisocoria In the second step, the results were used to compute the intersubject mean values and SDs. Linear regression was applied to the results from the first analysis step to illustrate the effect of age on the pupil diameter. The second stage provides information about the distribution of pupil parameters (diameter, fluctuations, anisocoria) in normal eyes.

To illustrate the relative change in static pupil diameters for normal eyes, the relative pupil contractions were calculated from the mean pupil diameters. The relative pupil contractions refer to intrasubject differences between the pupil diameters of the same eye at different illuminations divided by the pupil diameter at the lower illumination brightness.

The mean values for the intrasubject SDs (SD1) were calculated to assess the repeatability of the static pupillometry with PupilX. These mean values reflect the variability within the 5 consecutive measurements of pupil diameter. In contrast, the mean values of STD reflect the fluctuations during data acquisition for each illumination setting and eye (right/left).

Results

The mean age of the 91 successfully measured subjects was 39.7 years (SD 16.4 years, median 36 years). The mean and SD of the pupil diameters measured with PupilX, the repeatability calculated from the 5 consecutive measurements, the mean of the SDs calculated by the pupillometer’s software for each of the 5 consecutive measurements, and the internal consistency expressed as Cronbach α are shown in Table I for both eyes. The mean pupil diameters are calculated based on the whole dataset, while the Cronbach α and repeatability only use the data from subjects who were measured within 1 session. The number of subjects measured within 1 session is 71, 72, and 73 for 0 lx, 1 lx, and 16 lx, respectively.

Table I

The mean pupil diameters for scotopic, mesopic, and photopic illumination measured with PupilX in normal subjects

Brightness, lx	Mean d, mm	SD d, mm	Mean SD1, mm	Mean SD_pX, mm	Cronbach α
Left eyes
0	6.47	1.28	0.13	0.08	0.999
1	5.49	1.15	0.14	0.15	0.995
16	4.03	0.85	0.15	0.18	0.992
Right eyes
0	6.48	1.23	0.10	0.08	0.999
1	5.50	1.11	0.16	0.14	0.995
16	4.03	0.81	0.15	0.15	0.992

d = Pupil diameter; SD = standard deviation; SD1 = repeatability (standard deviation calculated from 5 consecutive measurements); SD_pX = standard deviation as reported by PupilX.

To compare the pupil diameters for left and right eyes, we compared the mean diameters of the pupils of left and right eyes, and present the result of the mean anisocoria. In the normal population, the differences between static pupil diameters of both eyes are very small. The mean pupil diameters for right and left eyes were identical within measurement precision (Fig. 2, Tab. I). The same applies to the median pupil diameters. The median pupil diameters were 6.69 mm, 5.50 mm, and 3.95 mm for the right eye under scotopic, mesopic, and photopic illumination, respectively. The corresponding median values of the pupil diameter for the left eye were 6.67 mm, 5.76 mm, and 4.05 mm. The mean unsigned anisocoria is 0.26 mm (SD 0.32 mm, median 0.17 mm) under scotopic, 0.26 mm (SD 0.27 mm, median 0.23 mm) under mesopic, and 0.19 mm (SD 0.19 mm, median 0.14 mm) under photopic illumination.

Fig. 2

The pupil diameters for scotopic, mesopic, and photopic illumination. Left eyes are shown in light gray, right eyes in dark gray. The extreme values are displayed as open circles or asterisks.

The static pupil diameter decreases with increasing illumination brightness. The mean pupil diameter decreased by 1.0 mm (SD 0.1 mm) from scotopic to mesopic, 1.5 mm (SD 0.1 mm) from mesopic to photopic, and 2.4 mm (SD 0.1 mm) from scotopic to photopic illumination. On average, the pupil diameter decreased from scotopic to mesopic illumination by 15% (median 14%) and from scotopic to photopic illumination by 37% (median 39%) (Tab. II).

Table II

The relative pupil contractions measured with PupilX in normal subjects

	(Scotopic − mesopic)/scotopic, %	(Scotopic − photopic)/scotopic, %	(Mesopic − photopic)/mesopic, %
Left eyes
Mean	14.6	36.7	26.1
SD	9.6	11.3	7.4
Median	13.8	39.3	27.2
Right eyes
Mean	14.5	36.6	26.1
SD	9.3	11.3	7.4
Median	13.9	39.3	27.2

Relative decrease in pupil diameter from scotopic to mesopic, scotopic to photopic, and mesopic to photopic illumination.

SD = standard deviation.

Linear regression on the mean pupil diameters was used to illustrate the age dependency of the pupil diameters as measured with PupilX in normal subjects (Fig. 3). Only subjects aged ≥20 years were included in the regression. The mean pupil diameter decreased with increasing age for all 3 illumination settings. The slope of the linear regression was smallest for photopic and largest for scotopic illumination (Tab. III).

Fig. 3

Pupil diameters as a function of age for scotopic (A), mesopic (B), and photopic (C) light conditions. The results of the regression analysis are shown in Table III.

Table III

The slopes and intercepts of the pupil diameters measured by PupilX in normal subjects as a function of age for subjects aged ≥20 years

Brightness, lx	S, μm/y	SE S, μm/y	I, mm	SE I, mm	R²
Left eyes
0	-58	3	8.8	0.1	0.47
1	-47	3	7.4	0.1	0.37
16	-26	2	5.1	0.1	0.21
Right eyes
0	-57	3	8.8	0.1	0.49
1	-44	3	7.4	0.1	0.36
16	-23	2	5.0	0.1	0.19

I = intercept; R² = goodness of the linear regression; S = slope; SE = standard error.

We then looked at the variability in the measurements. For both eyes, the differences among each of the 5 consecutive measurements with identical illumination were small compared to the differences between pupil diameters at different illuminations, as indicated by the high Cronbach α >0.99. The SD between consecutive measurements (mean SD1) (repeatability) was comparable to the mean of the SDs calculated by the pupillometer within each measurement of 90 frames (mean SD1) (Tab. I). The repeatability was better than 0.2 mm for all 3 illumination settings.

Discussion

There is no standardized protocol for pupil diameter measurements. Thus, comparison with measurements in other publications is difficult. The brightness levels for scotopic, mesopic, and photopic illumination, the method of illumination, the field of view, and the spectrum of the light source vary among available studies. Although the PupilX is capable of providing illumination levels of up to 1,000 lx, we decided to use only 16 lx maximum illumination to facilitate comparison with older instruments that are not capable of such high illumination levels such as the Procyon pupillometer (8). The indirect illumination of the pupil with white light by PupilX results in higher pupil diameters compared to direct illumination (8). Indirect illumination can be considered more natural than direct pupil illumination. Some research indicates that monocular and binocular pupillometry might result in different pupil size measurements (20, 21). The PupilX is capable of measuring the pupil response to illumination for either each eye separately or both eyes at once. With the possibility for both monocular and binocular pupil diameter measurements, the device might be able to shed more light onto this question. For the measurements at hand, only binocular illumination was used, as it is the natural form of illumination. The spectrum of the white light LED used for pupil illumination and stimulation contains an excess of blue light compared to normal daytime illumination (18). The blue light component of the illumination could reduce the amplitude of pupillary contraction for young subjects (<46 years) and increase the amplitude for older subjects compared with daylight (22).

Both eyes showed almost identical results. Average anisocoria was ≤0.26 mm. It was higher for scotopic than for photopic light conditions. This is in accordance with previous findings (23 -25). Greater variations and average extent of anisocoria could be seen in dark conditions.

Age is one of the confounding factors in the study of static pupil diameters. Older subjects, on average, have smaller pupil diameters than younger subjects (2). Previous studies with the same pupillometer using measurements of 96 subjects with a mean age of 51.7 years (SD 21.4 years) (8) resulted in mean scotopic pupil diameters that are smaller than our results obtained with a younger group of subjects aged 39.7 years (SD 16.4 years). Schilde et al (8) used a scotopic illumination of 0.06 lx as opposed to 0 (total darkness) in this study, which also might have contributed to the reduced scotopic pupil diameters previously reported. In a recent study using the PupilX pupillometer for the measurement of normal subjects, Rickmann et al (24) reported a mean pupil diameter of 5.39 ± 1.04 mm at 0 lx illumination. This is lower than our measurements. The difference can partially be explained by age differences. Our subjects were on average 12.2 years younger. Based on a first-order estimation using the slope calculated from the age dependence, one would expect 0.7 mm higher mean scotopic pupil diameter.

The influence of age was most apparent in the pupil diameter under weak (scotopic) illumination. The decrease in pupil diameter with increasing age for subjects older than 20 years (indicated by the slope of the linear regression) was smallest under high illumination and largest under low illumination. Thus, the range of pupillary contraction decreased with age. This qualitative observation agrees well with previous research (2). Pupil diameters of subjects younger than 20 years are expected to be increasing with age (26) and were excluded from the regression analysis.

The repeatability and mean SD was best for scotopic illumination. This is mainly for physiologic reasons, since fully dilated pupils display less pupillary unrest or hippus (13). Variations in the direction of sight during data acquisition could potentially affect the illumination of the pupil and thus the pupillary contraction under mesopic and photopic illumination conditions. The stability of the illumination settings might also play a role, but could not be studied here. Repetitive measurements under identical brightness conditions with the infrared pupillometer show good repeatability, with a SD <0.2 mm for illumination with 0 lx, 1 lx, and 16 lx. Under scotopic illumination, this seems superior to the repeatability of the widely used Procyon digital pupillometer as reported by Wickremasinghe et al (27). They did not measure the repeatability for the Procyon pupillometer for illumination with 1 lx and 16 lx. Eyes where it was not possible to collect 5 valid measurements in a single session were excluded from the repeatability analysis. Blinking artefacts caused the most problems. This is expected to induce no relevant bias (<0.01 mm, based on the analysis of the average SD of the included/excluded eyes). The repeatability may also vary with age of the subjects.

In addition to differences in the pupillary response due to age (2, 28), accommodation (3), and cognitive effects (7), individual differences may also be due to the anatomy of the iris, where the thickness might play a role. A reduced thickness is associated with reduced contraction amplitude for healthy subjects (28). The subjects for this study were recruited in Germany. The normal values reported here might only be valid for people of the same ethnicity. The eyes under study showed a wide range of pupil diameters for identical illumination conditions, which is also reflected in a wide range of relative pupil contraction amplitudes. The differences in age contribute to the wide distribution, but even after correction for their effect, substantial differences remain between the pupil sizes of individual subjects. Hashemi et al (29) found correlations between pupil diameter measured with Orbscan II and anterior chamber depth, age, and spherical equivalent. There are no significant differences between average scotopic or photopic pupil diameters in men and women (29, 30). Consequently, no distinction has been made according to sex within this study. However, the reduction of pupil size with age could be different between men and women (29).

Individual assessment of pupil size and dynamics along with other ocular characteristics will allow further IOL customization to each patient (14). Patients with large pupils may benefit more from aspheric IOLs, because uncorrected spherical aberration can cause significant image deterioration (31). The asphericity of aspheric IOLs should ideally be chosen according to the aberrations calculated from the central part of the cornea that corresponds with the entrance pupil. Multifocal IOLs with concentric refractive ring design may benefit from a central zone that is smaller than the photopic pupil diameter (32). In many cases, the postoperative pupil is significantly smaller than the preoperative pupil (33, 34). The preoperative pupil size has limited ability to assist the choice of well-suited refractive multifocal or aspheric IOLs.

The ablation zone for refractive surgery should be smaller than the maximum scotopic pupil size. In refractive corneal surgery, the postoperative pupil size will be different from the preoperative pupil size, because of changes in the corneal refractivepower. The postoperative pupil diameter measurement will be larger than the preoperative pupil diameter measurement for hyperopia treatment and smaller for myopia treatment (35).

We reported pupil diameters under static, binocular illumination measured with the infrared pupillometry PupilX in normal subjects. The PupilX is able to measure monocular and binocular pupil diameter under a variety of indirect illumination settings, even in total darkness. The device is capable of measuring the pupillary response to static or dynamic illumination. We reported the pupil diameter under static illumination. The measurements could be performed with repeatability (SD) better than 0.2 mm.

In order to use pupil diameter measurements for screening and risk assessment for ocular diseases, a standardized measurement protocol together with reliable normative data is desirable. The range of pupil parameters in the normal, healthy population can be used as a reference. This study adds information on normal data for measurements of static pupil diameters as made with the PupilX pupillometer under illumination with 0 lx, 1 lx, and 16 lx.

Footnotes

Disclosures

Financial support: Funding provided through a scholarship (A/11/86522) granted to the author’s study (E.C.) from the German Academic Exchange Service (DAAD) and the Dr. Rolf M. Schwiete Foundation (E.J.).

Conflict of interest: None of the authors has conflict of interest with this submission.

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